Establishment and new hosts of the non-native seed beetle Stator limbatus (Coleoptera, Chrysomelidae, Bruchinae) on acacias in Europe

A peer-reviewed open-access journal

NeoBiota 70: 167—192 (2021) i
doi: 10.3897/neobiota.70.7044 | RESEARCH ARTICLE %) N eoBiota

https:/ / neobi ota. pen soft. net Advancing research on alien species and biological invasions

Establishment and new hosts of the non-native seed
beetle Stator limbatus (Coleoptera, Chrysomelidae,
Bruchinae) on acacias in Europe

Arturo Cocco', Giuseppe Brundu', Cyril Berquier*®,
Marie Cécile Andrei-Ruiz*®, Michelina Pusceddu!, Marco Porceddu?%,
Lina Podda?*, Alberto Satta', Yohan Petit®*®, Ignazio Floris!

| Department of Agricultural Sciences, University of Sassari, Viale Italia 39, Sassari, Italy 2 Observatoire
Conservatoire des Insectes de Corse (OCIC), 14 Avenue Jean Nicoli, Corte, France 3 Department of Life and
Environmental Sciences, Centre for the Conservation of Biodiversity (CCB) University of Cagliari, Viale S.
Ignazio da Laconi 13, Cagliari, Italy 4 Sardinian Germplasm Bank (BG-SAR), Hortus Botanicus Karalitanus
(HBK), University of Cagliari, viale S. Ignazio da Laconi 9-11, Cagliari, Italy § Conservatoire Botanique
National de Corse (CBNC), 14 Avenue Jean Nicoli, Corte, France 6 Office de l'Environnement de la Corse
(OEC), 14 Avenue Jean Nicoli, Corte, France

Corresponding author: Arturo Cocco (acocco@uniss.it)

Academic editor: Alain Roques | Received 26 June 2021 | Accepted 20 October 2021 | Published 17 December 2021

Citation: Cocco A, Brundu G, Berquier C, Andrei-Ruiz MC, Pusceddu M, Porceddu M, Podda L, Satta A, Petit Y,
Floris I (2021) Establishment and new hosts of the non-native seed beetle Stator limbatus (Coleoptera, Chrysomelidae,
Bruchinae) on acacias in Europe . NeoBiota 70: 167-192. https://doi.org/10.3897/neobiota.70.70441

Abstract

Stator limbatus is a phytophagous beetle native to warm regions of North and Central America, feeding on
Fabaceae seeds and one of the most polyphagous species within the subfamily Bruchinae, here reported for
the first time in Europe and on new hosts. Adult beetles emerged from Acacia spp. seeds collected in the
islands of Corsica (France), and Sardinia (Italy). The wide presence in Sardinia and Corsica supports the
hypothesis that this alien species was introduced several years ago. In both islands, S. dimbatus emerged
from Acacia mearnsii seeds, with infestation rates of up to 74.2 and 90.8% in 2019 and 2020, respectively.
This seed beetle also emerged from two previously unreported host species, Acacia saligna and A. pycnan-
tha, showing highest infestation rates of 4.0 and 95.1%, respectively. Both Acacia species are reported as
new host associations with S. /imbatus. Overall, seed infestation rates recorded in 2019 and 2020 indicate
that S. Limbatus is well established and that Mediterranean bioclimatic conditions are suitable for its popu-
lation increase in size. This study lays the foundations for further research on known and potential host

species and the spread and distribution of S. imbatus in Europe.

Copyright Arturo Cocco et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY
4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

168 Arturo Cocco et al. / NeoBiota 70: 167—192 (2021)

Keywords
Acacia mearnsii, Acacia pycnantha, Acacia saligna, alien species, bean weevil, biological invasion, Mediter-

ranean islands

Introduction

The global movement of people and goods and climate change are dramatically pro-
moting the introduction of alien species in non-native environments in the Anthro-
pocene (Kueffer 2017), resulting in a continuous accumulation of these species world-
wide (Seebens et al. 2017; Venette and Hutchison 2021). This indicates that current
measures to avoid new introductions of alien species are not always effective. Therefore,
prevention, continuous monitoring in priority sites, early detection, and rapid inter-
vention are of major importance for avoiding the establishment of new invasive alien
species and agricultural or forestry pests and for reducing the spread of the existing
ones, with special concern towards protected areas and natural ecosystems.

Among seed-feeding insects, the subfamily Bruchinae (Coleoptera, Chrysomeli-
dae) beetles, renowned as bean weevils, is highly specific and likely the most impor-
tant (van Klinken 2005). This family includes about 4,350 taxa distributed worldwide
(Borowiec 1987). The beetle Stator limbatus (Horn, 1873) (Coleoptera, Chrysomelidae:
Bruchinae) is an endophagous seed feeder of legumes (Fig. 1). Its native range spans
from semiarid and xeric regions of southwestern United States and northern Mexico
to dry tropical forests of Central America and northern South America. Stator limbatus

A B

1mm

Figure |. Habitus of adult Stator limbatus A dorsal and B lateral view.

Establishment and new hosts of Stator limbatus in Europe 169

has a generalist habit and a wide host range, as it has been collected from > 90 host
plant species (de Jestis Parra-Gil et al. 2020), including many species of the genus Aca-
cia s.|. In its native range, it affects mostly native species, but also about 20 non-native
species (Stillwell et al. 2007). Despite that, host colonization of S. imbatus populations
varies greatly among regions, and distinct populations exhibit host specialization at a
local scale (Morse and Farrell 2005a, 2005b). Beetle populations are known to express
phenotypic plasticity to host species by adapting pre-imaginal development time and
body and egg size (Amarillo-Suarez and Fox 2006; Amarillo-Suarez et al. 2017).

Eggs are oviposited on mature seeds inside of dehiscent or partially dehiscent pods
when they are still on the plant Johnson 198 1a; Kingsolver 2004). Females usually lay
one egg per seed, and newly hatched larvae burrow into the seed integument beneath
the egg, complete their development and pupate inside the same seed. In the case in
which seeds are limiting, more eggs are deposited across a seed (Morse and Farrell
2005a). Beetles emerge from seeds as adults, mate and females start ovipositing within
24—48 hours, under laboratory conditions. Adults are facultatively aphagous, as they
only require resources acquired during the pre-imaginal stage to complete develop-
ment and reproduce (e.g. capital breeders) (Stillwell and Fox 2009). The generation
time at 28 °C was determined to be 28-30 days (Amarillo-Suarez and Fox 2006).

Several species within the S. imbatus host range, such as Acacia mearnsii De Wild
and Acacia saligna (Labill.) H.L.Wendl. native to Australia, have shown in Europe in-
vasive potential and negative impacts on native species, to the extent that containment
measures have been implemented (Lowe et al. 2000; European Union 2014; Tozzi et
al. 2021). Therefore, monitoring the presence of seed beetles of invasive Acacia spp.
in Europe is relevant in the perspective of finding and evaluating potential natural
enemies able to slow the expansion and mitigate the adverse impacts of those species.
Since Acacia in the broad sense have been grouped into distinct genera, e.g., Mari-
osousa, Vachellia, and Senegalia, and also other host species in the Leguminosae have
been synonymized or renamed, a dedicated study would be required to define the cur-
rent host range of the bruchid with valid plant names.

Outside its native range, S. limbatus has been reported in Hawaii (Bridwell 1920),
South America (Oliveira and Costa 2009; Romero Gomez et al. 2009; Meiado et
al. 2013), South Africa (Rink 2013), Iran (Boroumand 2010; Ghahari and Borowiec
2017), and United Arab Emirates (Delobel 2011), whereas reports from Mauritius,
Saudi Arabia, Yemen, and Oman were unconfirmed (Rink 2013).

In the framework of an international project assessing the risk of invasion of se-
lected alien species (ALTEM) (Inghilesi et al. 2018), some Acacia spp. seeds were tested
in a germination test during which several individuals of S. limbatus adults emerged
from seed lots of A. mearnsii seeds collected in Corsica (France) and Sardinia (Italy) in
2018. This insect species has not been yet recorded in Europe, so that new field collec-
tions were planned and carried out in 2019 and 2020.

The main aim of the present study was to investigate the establishment of S. Limba-
tus in Sardinia and Corsica according to the traits described by Yus-Ramos et al. (2014)
for alien seed beetles, as well as its host association and infestation levels. In addition,
a literature search analysis was carried out to provide an updated inventory of host

170 Arturo Cocco et al. / NeoBiota 70: 167—192 (2021)

species of S. imbatus with valid names, as understanding and predicting host shifts on
other Acacia species is of pivotal importance in order to define its potential distribution
in the Mediterranean Basin.

Materials and methods

Literature search analysis

Data sources used for investigating and updating the host range of S. Limbatus were re-
trieved from major online databases, such as Google Scholar, Web of Science, Scopus,
CAB abstracts, and ResearchGate. Papers were directly requested to authors and public
repositories and libraries whenever inaccessible online. Different combinations of key-
words were used in the literature search related to S. dimbatus and its host range. When-
ever possible, references were cross-checked and duplicates removed, giving priority
to older records. Original plant names were collected from each reference, whereas
country and locality records were reported whenever available.

Plant names were cross-checked taking into account relevant literature and differ-
ent on-line databases, in particular Seigler et al. (2006), Kyalangalilwa et al. (2013),
The Legume Phylogeny Working Group (LPWG 2017), World Flora Online (WFO)
(2020), Plants of the World Online (POWO 2020), BHL (for original protologues),
and the International Plant Name Index (IPNI) (2020). To our best knowledge, the
accepted nomenclature was followed according to current taxonomic standards.

Seed collection

Legumes and loments (hereafter pods) with seeds of A. mearnsii were manually col-
lected from adult trees naturalized in Corsica and Sardinia in September-November
2019. Seed sampling was carried out in Sardinia within two Special Areas of Conserva-
tion (SACs): “Berchida e Bidderosa” (Natura 2000 code ITB020012) (central eastern
Sardinia) and “Monte Linas — Marganai” (Natura 2000 code ITB041111) (southwest-
ern Sardinia), where the most important populations of A. mearnsii are located and the
species shows clear invasive traits outcompeting with native vegetation. On the other
hand, seeds in Corsica were collected along the eastern side of the island (Fig. 2). In
Sardinia, seed sampling was extended to other Acacia species, i.e., Acacia pycnantha
Benth. and A. saligna, not previously reported as host species but located nearby the
sampling sites of A. mearnsii. Following the emergence of S. Limbatus adults from all
Acacia species sampled in 2019 (See Results), field collection of seeds was repeated in
August-early September 2020 on the same species.

Acacia saligna is a widespread tree species in Corsica and Sardinia (Lozano et al.
2020), in particular along the coast, and severely impacts the characteristics of soils
and diversity and structure of the Mediterranean shrublands (Celesti-Grapow et al.
2016; Tozzi et al. 2021). The other two Acacia species, although common, are much

Establishment and new hosts of Stator limbatus in Europe val

@ A. mearnsii

©@ A. pycnantha

A, saligna

Figure 2. Map of sampling sites of Acacia spp. pods and seeds in Sardinia (Italy) and Corsica (France).

less widespread and form dense populations only in a limited number of sites. The
width of the sampling site varied widely, ranging from a single tree to tree stands larger
than 1,500 m’, as well as the seed production of trees. Therefore, a minimum of 20
pods per tree, representative of seed production, were collected at random from 1-30
randomly-chosen trees. All in all, the sample size ranged from 75 to 8,500 seeds, de-
pending on the width of the sampling site. In fact, seed production was generally very
large in all the investigated Acacia spp. in both years and was not a limiting factor in
seed sampling.

12 Arturo Cocco et al. / NeoBiota 70: 167—192 (2021)

Seed examination

The collected pods and seeds were stored at laboratory temperature in cardboard envelopes
sealed with adhesive tape, to avoid mold development and the escape of tiny seed beetles.
Envelopes were opened after approximately three months and beetles were separated and
identified morphologically using identification keys for S. imbatus adult detection (John-
son 1963; Kingsolver 2004). Seeds were further inspected under a dissecting microscope
and the number of Acacia spp. seeds with emergence holes was determined in order to cal-
culate the rate of infestation. Seeds of A. saligna showed very low seed infestation rates (see
Results). However, in view of its importance as an invasive species and in order to point out
a potential host shift, the presence of S. limbatus eggs on A. saligna seeds was also recorded.

Data analysis

The infestation rate, i.e., the percentage of seeds with S. /imbatus emergence holes, as
well as the percentage of A. saligna seeds with S. limbatus eggs were compared between
sites or host species by Fisher exact test. The seed infestation rates were preliminary
tested for data overdispersion by analyzing the y* approximation of the residual vari-
ance (Venables and Ripley 2002; Zuur et al. 2009). Since overdispersion of data was
found, overdispersion parameters were included in the corrected models using a quasi-
binomial distribution followed by type II ANOVA to test for significance of main
effects (Zuur et al. 2009). The seed infestation rate was the response variable, whereas
“sampling area’ and “year” were the fixed effects in 2019 and 2020, respectively. Cor-
rected analyses were conducted using R software version 4.1.0 (R Development Core
Team 2021) at the significance level of 0.05.

Results

Literature search analysis

The literature search on S. limbatus host plant species retrieved about 150 references.
After a careful nomenclatural revision, the host range of S. imbatus, as so far described
in literature, includes 37 plant genera belonging to three of the six subfamilies in the
family Fabaceae:

subfamily Caesalpinioideae: Acacia (16 species), Acaciella (2), Albizia (10), Caesalpinia
(1), Calliandra (4), Cassia (4), Cercidium (4), Chloroleucon (2), Delonix (1), Des-
manthus (1), Ebenopsis (2), Enterolobium (2), Havardia (4), Hesperalbizia (1), Leu-
caena (3), Lysiloma (4), Mariosousa (4), Mimosa (1), Neptunia (1), Painteria (1),
Parkinsonia (3), Piptadenia (2), Pithecellobium (5), Prosopis (5), Pseudopiptadenia
(1), Pseudosamanea (1), Senegalia (15), Sphinga (1), Vachellia (2), Wallaceodendron
(1), and Zapoteca (1);

Establishment and new hosts of Stator limbatus in Europe 13

subfamily Cercidoideae: Bauhinia (1);
subfamily Papilionoideae: Arachis (1), Butea (1), Erythrina (1), Glycine (1), and Sesbania (1).

Most host species belong to the subfamily Caesalpinioideae (105), 96 of which
to the clade mimosoid, followed by Papilionoideae (5) and a single species of Cerci-
doideae. The list also comprises the following eight species included as non-host, ex-
perimental hosts and uncertain reports: Calliandra humilis Benth., Cercidium texanum
A.Gray, Delonix regia (Bojer ex Hook.) Raf., Prosopis juliflora (Sw.) DC., Prosopis velu-
tina Wooton, Senegalia ataxacantha (DC.) Kyal. & Boatwr (syn. A. ataxacantha DC.),
Vachellia constricta (Benth.) Seigler & Ebinger, and Vachellia farnesiana (L.) Wight &
Arn. (Bridwell 1920; Johnson 1981b; Fox et al. 1996, 2006; Kingsolver 2004; Rink
2013). The comprehensive host range of S. imbatus is provided with up-to-date no-
menclature of host species on Table 1.

Seed infestation

The field surveys carried out in 2019-2020 demonstrated the presence of the seed-
feeding beetle S. dimbatus both in Sardinia (Italy) and Corsica (France) islands on the
host plant A. mearnsii (Table 1). In Sardinia, the beetle emerged from seeds collected
in all the 14 sites in both the central eastern and southwestern sampling areas. In
2019, the infestation rates ranged from 24.3 to 74.2% and from 39.3 to 83.4% in
Berchida-Bidderosa and Monte Linas — Marganai areas, respectively, showing significant
differences among sampling sites (Fisher tests: y7 = 1074.85; df= 5; P< 0.001 and y’ =
404.83; df= 7; P< 0.001, respectively) (Table 1). Overall, the seed infestation rate by
S. limbatus did not differ between central eastern and southwestern sampling areas (F
= 0.496; df= 1.13; P = 0.494). In 2020, the infestation in the central eastern sampling
sites also differed significantly among sites (range = 85.4—90.8%) (Fisher test: y* =
31.42; df=5; P< 0.001), and increased significantly compared to 2019 (F = 16.206; df
= 1.11; P= 0.002). A large majority of A. mearnsii seeds (2 96.5% of seeds sampled in
the various sites) showed S. limbatus eggs (up to 18 eggs in a single seed) and = 98.4%
of the infested seeds exhibited a single exit hole (Fig. 3A).

Acacia pycnantha trees sampled in central eastern Sardinia in both 2019 and 2020
(site 1) showed the highest infestation levels (85.1 and 95.1%, respectively) compared
to A. mearnsii sites in the same area (Table 1). Of A. pycnantha infested seeds sampled
in 2019 and 2020, 29.5 and 45.2%, respectively, exhibited two exit holes and up to
28 eggs were recorded in a single seed (Fig. 3B). Both the percentage of infested seeds
and seeds with two holes increased significantly from 2019 to 2020 (Fisher tests: y* =
48.73; df= 1; P< 0.001 and y* = 24.03; df= 1; P < 0.001, respectively).

Pods and seeds of A. saligna were collected in the surroundings of infested A. mearn-
sii and A. pycnantha trees in two and nine sites in central eastern Sardinia (Table 2).
The infestation rate was very low in both years and was significantly the highest at the
site 5 in both 2019 (4%) (Fisher test: y7 = 6.32; df= 1; P = 0.033) and 2020 (2.6%)
(Fisher test: y* = 53.74; df= 8; P< 0.001). However, S. limbatus eggs were recorded on

174

Arturo Cocco et al. / NeoBiota 70: 167—192 (2021)

Table |. Updated global host range of Stator limbatus following a literature search analysis and review of

valid plant names.

Host species Country (Locality)
Host plant valid name f Original name in the Reference References
Subfamily Caesalpinioideae
Acacia baileyana F.Muell. Acacia baileyana F. Mueller Johnson and Kingsolver 1976 USA (California)
Acacia confusa Mert. Acacia confusa Swezey 1928; Zacher 1952 USA (Hawaii)

Acacia cultriformis A.Cunn. ex
G.Don
Acacia cyclops A.Cunn. ex G.Don

Acacia cultriformis A.Cunn. ex
G.Don
Acacia cyclops

Johnson and Kingsolver 1976

Rink 2013

South Africa (Yzerfontein)

Acacia goldmanii (Britton & Rose)| Acacia goldmanii (Br. & Rose) Johnson 1979 Mexico

Wiggins Wiggins

Acacia koa A.Gray Acacia koa Swezey 1924 USA (Hawaii)
Acacia koa Gray Stein 1983 USA (Hawaii)

Acacia leptoclada Benth. Acacia leptoclada Romero Gomez et al. 2009

Acacia mangium Willd. Acacia mangium Willd. Pereira et al. 2004; Medina and Brazil (Mato Grosso,

Pinzén-Floridn 2011; Mojena et
al. 2018

Roraima), Colombia

Acacia mearnsii De Wild.

Acacia mearnsii De Wild.

Oliveira and Costa 2009; Cocco
et al. (present paper)

Brazil (Rio Grande do
Sul), France, Italy

Acacia mearnsii Fox et al. 2006; Rink 2013 South Africa (Tokai,
Western Cape)
Acacia melanoxylon R.Br. Acacia melanoxylon R.Br. Johnson and Kingsolver 1976
Acacia pycnantha Benth. Acacia pycnantha Benth. Cocco et al. (present paper) Italy

Acacia podalyriifolia A.Cunn. ex
G.Don

Acacia podalyriifolia A. Cunnin-
gham ex G.Don.

Garlet et al. 2011

Brazil (Rio Grande do Sul)

Acacia retinodes Schltdl.
Acacia retusa (Jacq.) R.A.Howard

Acacia retinodes Schlect.
Acacia retusa (Jacq.) R.A.Howard

Johnson and Kingsolver 1976
Johnson and Kingsolver 1976

USA (California)
Costa Rica

Acacia richii A.Gray Acacia richei (sic) (richii) Kingsolver 2004
Acacia saligna (Labill.) Acacia saligna (Labill.) Cocco et al. (present paper) Italy, France
H.L. Wendl. H.L.Wendl.
Acacia sp. Acacia sp. Johnson 1984; Boroumand 2010;} Guatemala, Iran (Bush-
Ghahari and Borowiec 2017 ehr), Mexico
Acaciella angustissima (Mill.) Acacia angustissima (Mill.) Johnson and Kingsolver 1976; Colombia, Mexico,
Britton & Rose Kuntze Johnson 1984, 1995 USA (Arizona, Texas),
Venezuela
Acacia angustissima Morse and Farrell 2005a Mexico, USA (Texas)
Acacia angustissima angustissima Kingsolver 2004
Acaciella goldmanii Britton & Acacia macmurphyi Wiggins Hetz and Johnson 1988 Mexico
Rose
Albizia adinocephala (Donn.Sm.) Albizzia (sic) (Albizia) adino- Janzen 1980 Costa Rica
Britton & Rose ex Record cephala
Albizia berteriana (DC.) Fawe. Pithecellobium fragrans Romero Gomez et al. 2009
& Rendle
Albizia berteroana (Balb. ex DC.) Albizia berteroana Romero Gomez et al. 2009
M.Gémez
Albizia caribaea (Urb.) Britton Albizia caribaea (Urban) Britton Johnson 1984 Honduras "
& Rose & Rose mn
Albizzia (sic) (Albizia) caribaea Janzen 1980 Costa Rica
Albizia caribaea Romero Gomez et al. 2009
Albizia niopoides var. niopoides Romero Gomez et al. 2009
Albizia chinensis (Osbeck) Merr. Albizzia (sic) (Albizia) chinensis Zacher 1952
Albizia julibrissin Durazz. Albizia julibrissin Fox et al. 2006
Albizia lebbeck (L.) Benth. Albizia lebbeck Benth. Lugo-Garcia et al. 2015 Mexico
Albizia lebbek (sic) lebbeck (L.) | Hetz and Johnson 1988; Johnson Mexico, Venezuela
Benth. 1995
Albizzia lebbek (sic) (Albizia Bridwell 1920 USA (Hawaii)
lebbeck)

Albizzia (sic) (Albizia) lebbeck
(L.) Benth.

Nascimento 2009

Brazil (Rio de Janeiro)

Establishment and new hosts of Stator limbatus in Europe

Host species

Host plant valid name +
Albizia saman (Jacq.) Merr.

Albizia saponaria Blume ex Migq.

Albizia sinaloensis Britton & Rose

Albizia sp.

Caesalpinia pulcherrima (L.) Sw.
Calliandra calothyrsus Meisn.
Calliandra eriophylla Benth.
Calliandra houstoniana (Mill.)
Stand.

Original name in the Reference

Samanea saman

Pithecolobium (sic) (Pithecello-
bium) (= Samanea) saman

Pithecellobium saman (Jacq.)
Merrill

References
Bridwell 1920; Morse and Farrell
2005a
Zacher 1952

Johnson 1984

V5
Country (Locality)
Panama, USA (Hawaii),

Venezuela

Guatemala

Pithecellobium saman (Jacquin)
Bentham

Johnson 1995

Ecuador, Venezuela

Pithecellobium saman
Samanea saman (Jacq.) Merrill
Albizia saponaria
Albizia sinaloensis Britt. & Rose

Albizia sp.
Caesalpinia pulcherrima

Calliandra calothyrsus Meissn.
Calliandra eriophylla Bentham

Janzen 1980
Johnson and Kingsolver 1976
Kingsolver 2004
Hetz and Johnson 1988; Johnson
1995
Johnson 1984, 1995

Fox et al. 2006
Johnson and Lewis 1993
Johnson 1979
Johnson 1984

Costa Rica
Costa Rica

Mexico

Brazil (Rio de Janeiro),
Ecuador, Honduras,
Venezuela

Nicaragua
USA (Arizona)

Mexico, Guatemala

Calliandra houstoniana vat.
calothyrsus (Meissn.) Barneby

Calliandra confusa Sprague &
Riley

Johnson 1984

Panama

Calliandra humilis Benth. ¢

Calliandra humilis var. reticulata
(A.Gray) L.D.Benson

Calliandra humilis ¢

Johnson 1981b

Calliandra humilis humilis
Calliandra humilis reticulata

Kingsolver 2004
Kingsolver 2004

Calliandra sp. Calliandra sp. Johnson and Kingsolver 1976; Costa Rica, Mexico,

Johnson 1984; Morse and Farrell Venezuela
2005a

Cassia fistula L. Cassia fistula Kingsolver 2004

Cassia grandis L.f. Cassia grandis Kingsolver 2004

Cassia javanica L. Cassia javanica javanica Kingsolver 2004

Cassia javanica subsp. nodosa Cassia javanica indochinensis Kingsolver 2004

(Buch.-Ham. ex Roxb.) K.Larsen

& S.S.Larsen

Cassia moschata Kunth * Cassia moschata Morse and Farrell 2005b

Cassia leiandya Benth. *

Cercidium floridum Torr.

Cercidium floridum subsp.
floridum
Parkinsonia florida
Cercidium torreyanum
Cercidium floridum Bentham

Romero Gomez et al. 2009

Kingsolver 2004; Fox et al. 2006
Zacher 1952
Johnson and Kingsolver 1976

USA (Arizona, California)

Cercidium floridum (Benth.) Fox et al. 1996, 2001; Stillwell USA (California)
and Fox 2005
Cercidium macrum 1.M.Johnst. Parkinsonia texana var. macra Romero Gomez et al. 2009
Parkinsonia texana macra Kingsolver 2004
Parkinsonia macra (Johnst.) Fox et al. 1996
Parkinsonia macra Nilsson and Johnson 1993 Mexico, USA (Texas)
Cercidium microphyllum Rose & | Cercidium microphyllum (Torr.) | Johnson and Kingsolver 1976 Mexico, USA (Arizona)
I.M.Johnst. Rose & Johnst.
Cercidium microphyllum (Benth.) Fox et al. 2001 USA (California)
Cercidium microphyllum Morse and Farrell 2005a USA (Arizona)
Parkinsonia microphylla Stilwell and Fox 2005
Cercidium texanum A.Gray = Parkinsonia texana texana Kingsolver 2004
Parkinsonia texana (A.Gray) Fox et al. 1996 USA (Texas)
S. Watson £
Cercidium sp. Cercidium sp. Johnson 1984 Mexico

176

Host species

Arturo Cocco et al. / NeoBiota 70: 167—192 (2021)

Host plant valid name +
Chloroleucon mangense (Jacq.)
Britton & Rose

Original name in the Reference
Chloroleucon mangense

Chloroleucon mangense (Jacquin)
Macbride

References
Morse and Farrell 2005b
Johnson 1995

Country (Locality)

Venezuela

Chloroleucon tenuiflorum (Benth.)
Barneby & J.W.Grimes

Delonix regia (Bojer ex Hook.)
Raf. §

Desmanthus bicornutus S.Watson

Pithecellobium scalare Griseb.
Delonix regia §

Desmanthus bicornutus

Johnson 1984
Kingsolver 2004

Kingsolver 2004

Brazil (Rio de Janeiro)

Ebenopsis confinis (Standl.) Britton
& Rose
Ebenopsis ebano (Berland.)

Ebenopsis confinis

Ebenopsis ebano

Romero Gomez et al. 2009

Romero Gomez et al. 2009

Barneby & J.W.Grimes Chloroleucon ebano Nilsson and Johnson 1993 USA (Arizona)
Pithecellobium ebano Kingsolver 2004
Siderocarpus flexicaule (sic) Cushman 1911 USA (Texas)
(Siderocarpos flexicaulis)
Ebenopsis sp. Siderocarpus (sic) (Siderocarpos) | Zacher 1952; Romero Gomez et

Enterolobium contortisiliquum
(Vell.) Morong

Enterolobium timbouva Mart.
Havardia acatlensis (Benth.) Brit-
ton & Rose

Havardia mexicana (Rose) Britton
& Rose

sp.
Enterolobium contortisiliquum
(Vell.) Morong
Enterolobium timbouva Mart.
Havardia acatlensis

Havardia mexicana
Pithecolobium (sic) (Pithecello-
bium) mexicanum FE. N. Rose

al. 2009
Meiado et al. 2013

Meiado et al. 2013
Romero Gomez et al. 2009

Romero Gomez et al. 2009
Johnson and Kingsolver 1976

Brazil (Pernambuco)

Brazil (Pernambuco)

Havardia pallens (Benth.) Britton | Pithecellobium pallens (Bentham) | Johnson and Kingsolver 1976 USA (Texas)
& Rose Standl.
Havardia pallens Morse and Farrell 2005a Mexico
Pithecolobium (sic) (Pithecello- Johnson and Kingsolver 1976
bium) brevifolium Bentham
Havardia sonorae (S.Watson) Havardia sonorae Romero Gomez et al. 2009
Britton & Rose Pithecellobium sonorae S. Wats. Johnson and Kingsolver 1976 Mexico
Hesperalbizia occidentalis (Brande- Albizia plurijuga Romero Gomez et al. 2009 Mexico
gee) Barneby & J.W.Grime Albizia occidentalis Brandegee Hetz and Johnson 1988
Leucaena diversifolia (Schltdl.) Leucaena diversifolia Romero Gomez et al. 2009
Benth. Acacia diversifolia Romero Gomez et al. 2009
Leucaena leucocephala (Lam.) Leucaena leucocephala (Lam.) Johnson 1984 Mexico
de Wit de Wit.
Leucaena leucocephala subsp. Leucaena leucocephala subsp. Romero Gomez et al. 2009
glabrata (Rose) Zarate glabrata
Leucaena pulverulenta (Schltdl.) Leucaena pulverulenta (Schl.) Johnson and Kingsolver 1976 USA (Texas)
Benth. Bentham
Leucaena trichandra (Zucc.) Urb. Leucaena diversifolia subsp. Romero Gomez et al. 2009
stenocarpa
Leucaena guatematlensis Britt. Johnson 1979 Mexico
& Rose
Leucaena guatematlensis (Britt. Hetz and Johnson 1988 Mexico
& Rose)
Lysiloma acapulcense (Kunth) Lysiloma acapulcense Romero Gomez et al. 2009 Mexico
Benth. Lysiloma acapulcensis (sic) (aca- Hetz and Johnson 1988 Honduras
pulcense) Bentham
Lysiloma acapulcensis (sic) (aca- Johnson 1984 Guatemala
pulcense) Kunth. Benth.
Lysiloma divaricatum (Jacq.) Lysiloma divaricata (Jacq.) Johnson and Kingsolver 1976; Mexico

J.EMacbr.

MacBride
Lysiloma divaricada (sic)
(divaricata)

Johnson 1984
de Lorea Barocio 2006

Lysiloma divaricatum

Romero Gomez et al. 2009

Lysiloma microphyllum

Romero Gomez et al. 2009

Establishment and new hosts of Stator limbatus in Europe

177

Host species Country (Locality)
Host plant valid name f Original name in the Reference References
Lysiloma latisiliquum (L.) Benth. | Lysiloma latisiliquum (L.) Benth. Johnson 1984 Mexico
Lysiloma tergeminum Benth. Lysiloma tergeminum Romero Gomez et al. 2009
Lysiloma watsonii Rose Lysiloma watsonii Romero Gomez et al. 2009
Lysiloma thornberi Britt. & Rose Johnson 1979 USA (Arizona)

Lysiloma thornberi

Zacher 1952

Lysiloma microphylla thornberi

Kingsolver 2004

Lysiloma microphyllum vat.

Romero Gomez et al. 2009

thornberi
Lysiloma sp. Lysiloma sp. Johnson and Kingsolver 1976; Costa Rica; Mexico
Johnson 1984
Mariosousa acatlensis (Benth.) Acacia acatlensis Bentham Johnson and Kingsolver 1976 Mexico
Seigler & Ebinger
Mariosousa coulteri (Benth.) Acacia coulteri Bentham Johnson and Kingsolver 1976 Mexico
Seigler & Ebinger Acacia coulteri Romero Gomez et al. 2009
Mariosousa coulteri Lugo-Garcia et al. 2015

Acacia near coulteri Bentham Johnson and Kingsolver 1976 Mexico
Mariosousa heterophylla (Benth.) Acacia willardiana Rose Johnson and Kingsolver 1976 Mexico
Seigler & Ebinger
Mariosousa millefolia (S.Watson) Acacia millefolia Wats. Johnson and Kingsolver 1976 USA (Arizona)
Seigler & Ebinger
Mimosa distachya vax. laxiflora Mimosa laxiflora Benth. Lugo-Garcia et al. 2015 Mexico
(Benth.) Barneby
Mimosa sp. Mimosa sp. de Lorea Barocio 2006; Romero Mexico

Gomez et al. 2009

Neptunia plena (L.) Benth. Neptunia plena Kingsolver 2004
Painteria leptophylla (DC.) Britton Painteria leptophylla (DC.) de Jesus Parra-Gil et al. 2020 Mexico

& Rose

Parkinsonia aculeata L.

Britton & Rose

Parkinsonia aculeata Linnaeus

Johnson and Kingsolver 1976

Mexico, USA (Arizona,

Texas)
Parkinsonia aculeata Morse and Farrell 2005a USA (Texas)
Acacia aculeata Zacher 1952
Parkinsonia florida subsp. peninsu- Cercidium floridum subsp. Romero Gomez et al. 2009
lare (Rose) J.E.Hawkins & Felger peninsulare
Parkinsonia praecox (Ruiz & Pav.) Parkinsonia praecox Romero Gomez et al. 2009
Hawkins Cercidium praecox (Ruiz & Pav.) | Johnson and Kingsolver 1976 Mexico
Harms
Piptadenia flava (Spreng. ex DC.) Piptadenia flava Janzen 1980 Costa Rica
Benth. Parkinsonia flava Romero Gomez et al. 2009
Piptadenia obliqua (Pers.) Piptadenia obliqua (Persoon) Johnson 1995 Venezuela
J.EMacbr. Macbride
Piptadenia oblique Morse and Farrell 2005a Venezuela

Pithecellobium candidum (Kunth) Pithecellobium candidum Johnson 1995 Ecuador

Benth. Bentham

Pithecellobium dulce (Roxb.) Pithecellobium dulce (Roxb.) Johnson and Kingsolver 1976; Colombia, Costa Rica,

Benth. Bentham Johnson 1984, 1995 Ecuador, El Salvador,

Guatemala, Honduras,
Mexico, Venezuela
Pithecellobium dulce Morse and Farrell 2005a; de Lorea} Mexico, Ecuador, Ven-
Barocio 2006 ezuela
Pithecolobium (sic) (Pithecello- Bridwell 1920; Zacher 1952 USA (Hawaii)
bium) dulce

Pithecellobium excelsum (Kunth) | Pithecellobium excelsum Bentham Johnson 1995 Ecuador

Mart. Pithecellobium excelsum Morse and Farrell 2005a Ecuador

Pithecellobium oblongum Benth. Pithecellobium oblongum Janzen 1980 Costa Rica

Pithecellobium unguis-cati (L.) Pithecellobium unguis-cati Morse and Farrell 2005a Venezuela

Benth. Pithecolobium unguiscatae (sic) Bridwell 1920 USA (California)

(Pithecellobium unguis-cati)

Senegalia gaumeri (S.F.Blake)

Acacia gaumeri Blake

Johnson 1984

178 Arturo Cocco et al. / NeoBiota 70: 167—192 (2021)
Host species Country (Locality)
Host plant valid name f Original name in the Reference References
Pithecellobium sp. Pithecellobium sp. Johnson and Kingsolver 1976 EI Salvador
Pithecolobium (sic) (Pithecel- Bridwell 1920 USA (Hawaii)
lobium) sp.
Prosopis chilensis (Molina) Stuntz Prosopis chilensis Romero Gomez et al. 2009
Prosopis chilensis (= juliflora) Zacher 1952
Prosopis farcta (Banks & Sol.) Prosopis farcta Boroumand 2010 Iran (Bushehr and Yazd)
J.EMacbr. Prosopis farcta (Banks & Soland.) Shamszadeh et al. 2017 Iran (Yazd)
Macbr.
Prosopis glandulosa var glandulosa | Prosopis glandulosa glandulosa Kingsolver 2004
Torr.
Prosopis glandulosa vat. torreyana Prosopis glandulosa torreyana Kingsolver 2004
(L.D.Benson) M.C.Johnst.
Prosopis juliflora (Sw.) DC. $ Prosopis juliflora + Bridwell 1920; Kingsolver 2004;
Fox et al. 2006
Prosopis velutina Wooton ¢ Prosopis velutina ¢ Johnson 1981b
Pseudopiptadenia inaequalis Piptadenia inaequalis Bentham Johnson 1995 Venezuela
(Benth.) Rauschert Piptadenia inaequalis Morse and Farrell 2005a Venezuela
Pseudosamanea guachapele (Kunth) Pseudosamanea guachapele Amarillo-Sudrez et al. 2011
Harms Albizia guachepele (sic) (guacha- Johnson 1995 Colombia
pele) (HBK.) Dugand
Senegalia ataxacantha (DC.) Kyal. Acacia ataxacantha ¥ Rink 2013 South Africa
& Boatwr +
Senegalia berlandieri (Benth.) Acacia berlandieri Bentham Johnson and Kingsolver 1976 Mexico, USA (Texas)
Britton & Rose Acacia berlandieri Amarillo-Suarez et al. 2011 USA (Texas)

Honduras, Mexico

Britton & Rose Acacia gaumeri Morse and Farrell 2005a Mexico

Senegalia gilliesii (Steud.) Seigler Acacia furcatispina Romero Gomez et al. 2009

& Ebinger

Senegalia glomerosa (Benth.) Acacia glomerosa Romero Gomez et al. 2009

Britton & Rose Acacia near glomerosa Bentham | Johnson and Kingsolver 1976 Mexico

Senegalia greggii (A.Gray) Britton Acacia greggii A. Gray Johnson and Kingsolver 1976 Mexico, USA (Arizona,

& Rose California, Texas)
Acacia gregeii Morse and Farrell 2005a; Ama- USA (Arizona)

rillo-Sudrez et al. 2011

Senegalia hayesii (Benth.) Britton Acacia hayesii Romero Gomez et al. 2009

& Rose

Senegalia occidentalis (Rose) Acacia occidentalis Rose Johnson and Kingsolver 1976 Mexico

Britton & Rose

Senegalia picachensis (Brandegee) | Acacia picachensis T. S. Brandg. Johnson 1984 Mexico

Britton & Rose
Senegalia polyphylla (DC.) Britton
& Rose

Acacia polyphylla DC.

Johnson 1995; Johnson and
Siemens 1995

Colombia, Venezuela

Senegalia riparia (Kunth) Britton
& Rose

Acacia riparia

Romero Gomez et al. 2009

Senegalia roemeriana (Scheele) Acacia roemeriana Scheele Johnson and Kingsolver 1976 USA (Texas)
Britton & Rose
Senegalia tamarindifolia (L.) Acacia tamarindifolia (L.) Johnson 1995; Johnson and Venezuela
Britton & Rose Willdenow Siemens 1995

Acacia tamarindifolia Morse and Farrell 2005a Martinique

Senegalia tenuifolia (L.) Britton
& Rose

Acacia tenuifolia (L.) Willd.

Johnson and Kingsolver 1976;
Johnson 1984

Costa Rica, Mexico

Senegalia wrightii (Benth.) Britton
& Rose

Sphinga platyloba (DC.) Barneby
& J.W.Grimes

Vachellia constricta (Benth.)
Seigler & Ebinger $

Acacia wrightii Bentham Johnson and Kingsolver 1976 USA (Texas)
Acacia wrightii Morse and Farrell 2005a Mexico, USA (Texas)
Sphinga platyloba Morse and Farrell 2005b
Pithecellobium platyloba (sic) Janzen 1980 Costa Rica
(platylobum)
Havardia platyloba Romero Gomez et al. 2009

Acacia constricta ¥

Johnson 1981b

Vachellia farnesiana (L.) Wight
& Arn.

Acacia farnesiana $

Bridwell 1920

Acacia farnesiana

Zacher 1952

Establishment and new hosts of Stator imbatus in Europe

Host species

Host plant valid name +
Wallaceodendron celebicum Koord.

Original name in the Reference

Wallaceodendron celebicum

References
Bryan 1932

179

Country (Locality)

USA (Hawaii)

Zapoteca portoricensis (Jacq.)
H.M.Hern.

Zapoteca portoricensis

Morse and Farrell 2005b

Subfamily Cercidoideae

Bauhinia purpurea L.
Subfamily Papilionoideae
Arachis hypogaea L.

Butea monosperma (Lam.) Kunze

Bauhinia purpurea L.

Arachis hypogaea
Butea monosperma
Erythrina monosperma

Fox et al. 2006

Kingsolver 2004
Romero Gomez et al. 2009
Zacher 1952

Erythrina sandwicensis O.Deg.

Erythrina sandwicensis

Kingsolver 2004

Glycine max (L.) Mert.

Glycine max

Kingsolver 2004

Sesbania sp.

Sesbania sp.

Romero Gomez et al. 2009

+ Valid names following Kyalangalilwa et al. (2013), Plants of the World Online (POWO 2020), and World Flora Online (WFO)
(2020). $ Non-host or experimental hosts. * Morse and Farrell (2005b) did not specify the authorship, it is therefore impossible to
determine whether they referred to Cassia moschata Kunth or Cassia leiandra Benth, which are both accepted names. § Uncertain report
(Kingsolver 2004).

up to 52.8 and 79.6% of A. saligna seeds in 2019 and 2020, respectively (Fig. 3C). A
single seed harbored up to six eggs. The seed infestation rate ranged in 2020 from 0 to
2.6% regardless of the distance from infested Acacia spp. trees, whereas A. saligna seeds
with the highest percentage of beetle eggs (sites 1, 4, 5, and 6, range 45.1—79.6%) were
recorded on trees <5 m apart from infested trees (Table 2).

In Corsica, S. limbatus adults were recorded in all four sampling sites. In 2019,
adults emerged in both eastern (site 19) and northeastern (site 18) sites from A. mearn-
sii seeds. Most seeds exhibited exit holes and egg chorions of S. Limbatus, although a
few individuals were recorded: four adults from site 19 and one from site 18. In 2020,
S. limbatus adults were further recovered in sites 18 and 21, in which more than 400

1mm

Figure 3. Acacia seeds (with arils on top) infested by Stator limbatus, with eggs and exit holes A S. limbatus
adult emerging from an Acacia mearnsii seed with 11 eggs B S. limbatus adult emerging from A. pycnantha

seed with two exit holes C A. saligna seed with a S. limbatus egg and one exit hole.

180 Arturo Cocco et al. / NeoBiota 70: 167—192 (2021)

Table 2. Locations of sampling sites in Sardinia (Italy) and Corsica (France), and seed infestation rates of

Acacia pycnantha and A. mearnsii by Stator limbatus.

Site no. WGS84 Coordinates (°N, °E) Sampling date Host plant Sampled seeds (no.) Infestation rate (%) f
Sardinia, Berchida-Bidderosa area, 2019

1 40.451995, 9.778190 18/09/2019 A, pycnantha 315 85.la
2 40.459980, 9.785646 18/09/2019 A. mearnsii 199 38.7 d
3 40.457190, 9.793082 18/09/2019, 01/10/2019 A. mearnsii 3459 74.2b
4 40.463992, 9.798704 18/09/2019, 01/10/2019 A. mearnsii 1030 49.3d
5 40.545390, 9.782090 18/09/2019 A. mearnsii 61 45.9d
6 40.549220, 9.788000 18/09/2019, 01/10/2019 A. mearnsii 1137 24.3e
7, 40.578073, 9.777057 18/09/2019, 01/10/2019 A. mearnsii 3639 67.5
Sardinia, Berchida-Bidderosa area, 2020

1 40.451995, 9.778190 10/08/2020 A. pycnantha 2415 95.1 a
2 40.459980, 9.785646 10/08/2020 A. mearnsii 1784 90.8 b
3 40.457190, 9.793082 10/08/2020 A. mearnsii 2234 89.0 bc
4 40.463992, 9.798704 10/08/2020 A. mearnsii 1704 86.5d
5 40.545390, 9.782090 10/08/2020 A, mearnsii 1023 85.4d
6 40.578073, 9.777057 10/08/2020 A. mearnsii 390 87.2 cd
7 40.549220, 9.788000 10/08/2020 A. mearnsii 1574 89.8 bc
Sardinia, Monte Linas — Marganai area, 2019

10 39.421480, 8.716520 23/09/2019 A. mearnsii 226 61.9 cde
11 39.398540, 8.695790 23/09/2019 A. mearnsii 199 54.3e
12 39.391094, 8.675427 23/09/2019 A. mearnsii 341 65.4 cd
13 39.396532, 8.658998 23/09/2019 A. mearnsii 671 66.6 c
14 39.393961, 8.663604 23/09/2019 A. mearnsii 980 59.8 de
15 39.391863, 8.669016 23/09/2019 A. mearnsii 951 7I.4b
16 39.420067, 8.713574 23/09/2019 A. mearnsii 1187 83.4 a
17 39.449340, 8.733530 23/09/2019 A. mearnsii 428 39.3
Corsica, 2019

18 42.546699, 9.525582 29/10/2019 A. mearnsii - n.a.
19 42.125300, 9.510656 07/11/2019 A. mearnsii - na.
Corsica, 2020

18 42.546576, 9.5246522 20/08/2020 A. mearnsii - n.a.
19 42.125065, 9.510606 20/08/2020 A. mearnsii 8500 56.0
21 41.380217, 9.222299 03/09/2020 A. mearnsii - na.

+ Different letters within years indicate significant difference by Fisher exact test (P< 0.05). n.a. = not available.

Table 3. Locations of sampling sites in Sardinia (Italy) and Corsica (France), and seed infestation rates of

Acacia saligna seeds by Stator limbatus.

Site no. WGS84 Coordinates (°N, °E) Sampling date Distance from in- Sampled Infestation Seeds with S. lim-
fested Acacia trees seeds(no.) rate (%) f batus eggs (%) t

Sardinia, Berchida-Bidderosa area, 2019

4 40.463799, 9.799295 18/09/2019 <5m 156 0b 44.9 a

5 40.545420, 9.782050 18/09/2019 <5m 75 4.0a 52.8 a

Sardinia, Berchida-Bidderosa area, 2020

1 40.451980, 9.778390 10/08/2020 <5m 1550 Od 57.2b

4 40.463799, 9.799295 10/08/2020 <5m 524 0.6 abc 60.7 b

5 40.545420, 9.782050 10/08/2020 <5m 116 2.6a 79.6 a
40.546396, 9.782224 10/08/2020 < 100m 864 0.3 bed 244d
40.546109, 9.781190 10/08/2020 < 100m 867 Od 18.0 e

6 40.549240, 9.788131 10/08/2020 <5m 859 Od 45.1c
40.549022, 9.786670 10/08/2020 < 100m 1237 0.2 bed 22.5d

8 40.618420, 9.743740 10/08/2020 > 100m 981 Od 3.0 ¢

9 40.592818, 9.710812 17/08/2020 > 100m 596 0.2 bed 8.9 f

Corsica, 2020

20 41.380217, 9.222299 27/08/2020 - 4360 0.2 n.a.

+ Different letters within years indicate significant difference by Fisher exact test (P < 0.05).

Establishment and new hosts of Stator limbatus in Europe 181

adults emerged from samples of A. mearnsii seeds of unknown sizes. In site 19, the
infestation level by S. Limbatus was 56.0%. Seeds of A. saligna were collected in site 20,
where the infestation rate was 0.2%.

Discussion

The extensive collection of S. dimbatus during the field surveys in 2019 and 2020 in
Sardinia and Corsica following the first record in 2018 indicates that the seed beetle
has found suitable climatic conditions and has established in Europe. Stator limbatus
can be considered established according to the definition of Yus-Ramos et al. (2014),
i.e., a species able to reproduce successfully in natural ecosystems. Stator limbatus ex-
hibits biological features that could support its further spread in Europe. At first, this
species has a wide host range worldwide, with about 15 species reported in Europe
(Euro+Med 2021; GBIF 2021). Furthermore, its native geographic range includes di-
verse climates, spanning from dry forests of northern South America to deserts of Cen-
tral America and southwestern United States (Stillwell and Fox 2009). In addition, this
bruchid developed under laboratory conditions also on non-native species, including
Acacia cyclops A.Cunn. G.Don and S. ataxacantha (syn. A. ataxacantha) (native to Aus-
tralia and South Africa, respectively) (Rink 2013), as well as non-host species, such as
C. humilis, C. texanum, P juliflora, P. velutina, V. constricta, and V. farnesiana (Bridwell
1920; Johnson 1981b; Fox et al. 1996). Finally, S. dimbatus have shown adaptive ovi-
position phenotypic plasticity in response to host species, as fewer and bigger eggs are
laid on exotic or unfavorable hosts (Amarillo-Suarez et al. 2017). Such maternal egg-
size plasticity is suggested to be an ancestral trait influencing the evolution of the diet
breadth (Amarillo-Sudrez and Fox 2006). Overall, the wide presence of host species of
S. limbatus in Europe, its strong host shift potential, and climate adaptation suggest its
possible spread in Mediterranean environments, and its presence in unsampled areas
cannot be ruled out.

This species was recovered from Acacia spp. seeds in Sardinia, in multiple sites dis-
tant up to 150 km, and Corsica, in four areas distant about 130 km. Even though the
country of first introduction in Europe remains undetermined, the wide presence of
this alien insect in distant areas supports the hypothesis that its introduction occurred
several years ago. The introduction of S. /imbatus in Europe was most likely accidental
and its detection unexpected. The pathway of first introduction is presently unknown,
as no specific custom interception has so far been reported. With regard to pathways
of secondary spread, in view of its wide host range and endophytic behavior of larvae,
we may assume that it was introduced through movement of contaminated commodi-
ties, i.e., plants for planting, as a parasite of seeds (CBD 2014; Faulkner et al. 2020).
In fact, after its first introduction, a secondary spread pathway may have occurred as
a result of movement of contaminated plants (with pods) or seeds of A. saligna, A.
mearnsii, and A. pycnantha, which are commonly planted in southern Europe and sig-
nificantly traded. In addition, the very large number of different host species should be

182 Arturo Cocco et al. / NeoBiota 70: 167—192 (2021)

taken into account (Table 1), as many are common ornamental, i.e., Albizia spp., Leu-
caena spp., Parkinsonia spp., and Glycine max (L.) Merr., or forestry and multipurpose
species, i.e., Acacia spp., in the Mediterranean area. Therefore, in order to investigate
the S. imbatus presence or intercept its introduction in areas nearby Sardinia and Cor-
sica, specific monitoring plans on its host species should be set up in southern France
and mainland Italy. Although the pathways of first introduction and secondary spread
are generally not known for bruchid seed beetles, several authors suggest introductions
through importation of seed or nursery stocks of host plant species for ornamental or
forestry purposes, e.g., Bruchidius terrenus (Sharp, 1886) on Albizia julibrissin Durazz.
and Amblycerus robiniae (Fabricius, 1781) on Gleditsia triacanthos L. in the United
States (Kingsolver 2004; Hoebeke et al. 2009; Yus-Ramos et al. 2014).

The introduction of alien seed beetles in Europe shows an increasing trend in
the last 20 years, in accordance with the worldwide trend described by Seebens et al.
(2017). Beenen and Roques (2010) reported 14 Bruchinae alien species in Europe,
seven of which introduced before 1900, three species in the period 1901-1950, two
in 1951-2000, and finally two species reported from 2001 to 2010. Yus-Ramos et al.
(2014) further extended the list of alien bruchids in Europe to a total of 42 species,
including four recent introductions, namely Bruchidius radiannae Anton & Delobel,
2003 and Caryedon acaciae (Gyllenhal, 1833) on Vachellia karroo (Hayne) Banfi &
Galasso (syn. Acacia karroo Hayne) in 2007 in Spain (Yus Ramos and Coello Garcia
2007, 2008), Acanthoscelides macrophthalmus (Schaeffer, 1907) on Leucaena leucoceph-
ala (Lam.) de Wit in Cyprus in 2007 (Vassiliou and Papadoulis 2008), and B. terrenus
on A. julibrissin in Bulgaria in 2009 (Stojanova 2010). Furthermore, A. robiniae was
reported on G. triacanthos in Romania in 2018 following an unconfirmed report in
Hungary in 1986 (Radac et al. 2021). Therefore, according to literature reports, seven
species of bruchids have been reported in Europe in the last 20 years. In both Corsica
and Sardinia, S. limbatus larvae developed on seeds of A. mearnsii, a tree native to
Australia which has shown to be invasive in Europe, South America, and Africa. This
insect-host association has been previously reported in Brazil, where an infestation rate
of 44.3% was observed (Oliveira and Costa 2009), and South Africa (Rink 2013).
Acacia mearnsii is cultivated in Brazil for tannins, cellulose, and charcoal production
(Garlet et al. 2011), whereas in Europe and in South Africa, presently, this species has
a lower significant economic importance and is rather invasive (Souza-Alonso et al.
2017; Railoun et al. 2021).

In Sardinia, beetle adults emerged abundantly also from A. pycnantha seeds, and,
interestingly, 45% of sampled seeds showed two exit holes, differently from A. mearnsii
seeds which showed a single exit hole. This brings evidence that A. pycnantha seeds sup-
port the development of more than one larva of S. /imbatus, most likely because of the
bigger size of its seeds compared to those of A. mearnsii. In central eastern Sardinia, the
infestation rate was more homogeneous among sampling sites in 2020 than in 2019,
as the range decreased from 49.9% (24.3-74.2%) in 2019 to 5.4% (85.4—90.8%) in
2020. Moreover, infestation rates increased significantly on both A. mearnsii and A.
pycnantha. However, the seed production of trees in the sampling sites was not quan-

Establishment and new hosts of Stator limbatus in Europe 183

titatively estimated being beyond the aims of the study. Estimates of seed infestation
rates with no assessment of tree seed production and over such a short period, i.e. two
years, prevent to infer on spatio-temporal population trends of S. limbatus. The same
insect abundance can, in fact, cause high infestation rates in the event of low seed pro-
duction or low rates when seed production is high. Nonetheless, although Acacia spp.
seed production and accumulation may vary widely, Australian and African species
usually produce large or very large quantities of seed and may have large soil-stored
seed banks (Gibson et al. 2011). High production of seeds for the three investigated
species has been observed both in the native and in the invaded ranges, e.g., A. mearnsii
in South Africa (Impson et al. 2021), being one of the drivers of invasiveness at the
global level. Indeed, large amounts of pods were observed on Acacia spp. trees as well
as seeds in the topsoil in both 2019 and 2020 (A. Cocco, Y. Petit, pers. obs.). Further-
more, high numbers of seedlings were observed in the sampling sites with A. mearnsii.

Previous studies on infestation by S. /imbatus on Fabaceae species reported seed
damages of 15% on E. timbouva (Meiado et al. 2013), 19% on Acacia mangium Willd.
(Mojena et al. 2018), and 70% on Acacia podalyriifolia A.Cunn. ex G.Don (Garlet
et al. 2011) in Brazil. In Mexico, seed infestation rates of 16.8% were observed on
Painteria leptophylla (DC.) Britton & Rose (de Jesus Parra-Gil et al. 2020) and 33.6%
on Mariosousa coulteri (Benth.) Seigler & Ebinger by both S. imbatus and Merobru-
chus santarosae Kingsolver, 1989 (Coleoptera, Chrysomelidae) (Romero Gomez et al.
2009). Susceptibility to S. limbatus widely varied among hosts and areas; however,
comparisons are difficult, as seed infestation rates are influenced by a number of abiotic
and biotic factors, including seed availability and environmental conditions. Despite
its recent report in South Africa, S. dimbatus has not been reported infesting A. pycnan-
tha seeds (Rink 2013; Magona et al. 2018).

A word of caution is in order with regard to A. saligna as a host species for S.
limbatus. In fact, infestation rates were very low in both years and countries, and the
highest values (4% in 2019 and 2.6% 2020) were observed in the same site. None-
theless, infestation by S. Limbatus on A. saligna seeds was not limited to a single site,
as infested plants were observed in both Sardinia and Corsica. Moreover, beetle eggs
were observed on up to 80% of A. saligna seeds, especially on plants near to infested
Acacia spp. trees. This could be due to an opportunistic egg-laying behavior on the
nearest alternative hosts. Furthermore, oviposition on A. saligna indicates that seeds
had no antixenotic effect on female oviposition and oviposition is promoted by suit-
able hosts nearby. Chemical or physical barriers on A. saligna seeds preventing larval
development cannot be ruled out and would require further investigations. Laboratory
tests carried out in South Africa investigating the oviposition preference showed that
S. limbatus females accepted A. saligna seeds for oviposition, together with seeds of A.
cyclops, A. mearnsii, Paraserianthes lophantha (Willd.) I.C.Nielsen (invasive non-native
species in South Africa), and Vachellia tortilis (Forssk.) Galasso & Banfi [syn. Acacia
tortilis (Forssk.) Hayne], S. ataxacantha, Senegalia caffra (Thunb.) PJ.Hurter & Mabb.
[syn. A. caffra (Thunb.) Willd.], Senegalia nigrescens (Oliv.) PJ.Hurter [syn. A. nigres-
cens (Oliv.)] and Vachellia sieberiana var. woodii (Burtt Davy) Kyal. & Boatwr. [syn. A.

184 Arturo Cocco et al. / NeoBiota 70: 167—192 (2021)

sieberiana vat. woodii (Burtt Davy) Keay & Brenan] (native species to South Africa).
However, adults emerged only from A. mearnsii, A. cyclops, and S. ataxacantha, indicat-
ing that food availability may not be the only factor limiting the larval development
(Rink 2013).

In view of its high seed infestation rates, S. /imbatus has been suggested to play a
role as biocontrol agent of invasive non-native Acacia species (Rink 2013). In South
Africa, extensive biological control programs have been developed against invasive
tree species, as, for example, the release of A. macrophthalmus for biological control
of L. leucocephala in 1999 (Olckers 2004). Five seed-weevil Melanterius spp. (Cole-
potera, Curculionidae) were introduced from Australia in different periods to reduce
the invasiveness of P lophantha and ten Acacia spp., including the three species inves-
tigated in the present paper, i.e., A. mearnsii, A. saligna, and A. pycnantha (Impson
et al. 2011). Seed damage caused by weevils varied largely among sites and years
from 4% to over 90%. Such variability was explained by a specific 4-year study on
Melanterius—Acacia relationship and was mostly due to variable seed quality that re-
sulted in low larval and pupal survival rates (Impson and Hoffmann 2019). Overall,
seed-feeders are unlikely to effectively reduce the Acacia spp. density as a stand-alone
control agent due to the extraordinarily high prolificacy of plants resulting in huge
accumulation of long-lived seeds in the soil. In fact, effective results were obtained
through the release of the flower-galling midge, Dasineura rubiformis Kolesik (Dip-
tera, Cecidomyiidae) complemented by a seed-feeding weevil, Melanterius maculatus
Lea (Coleoptera, Curculionidae), which caused a strong reduction of seed production
of A. mearnsii (Impson et al. 2021). This reduction is expected to curb the accumula-
tion rate of the seed banks and, in the medium-long term, reduce the spread of the
invasive species. Besides a potential biocontrol agent of invasive plant species, further
beneficial environmental effects by S. limbatus may be represented by the promotion
of seed germination, e.g., on Enterolobium contortisiliquum (Vell.) Morong and E.
timbouva Matt. (Meiado et al. 2013).

The present findings indicate the adaptability of S. Limbatus to new host species
when established in new areas. Stator limbatus also showed phenotypic plasticity in
response to seed size or seed quality (Amarillo-Sudrez and Fox 2006), in accordance
with findings in other species (Hardy et al. 1992; Tsai et al. 2001). Moreover, this is
consistent with results from studies showing that development time decreased and
adult mass increased when insects developed on high quality hosts (Lindroth et al.
1991; Stockhoff 1993). Therefore, host shifts on local plants and new host associations
cannot be ruled out in Europe in view of its ability to accept and adapt to local hosts.
Adaptation to new or non-preferred host species has been observed on other coleopter-
an alien species, such as the red palm weevil Rhynchophorus ferrugineus (Olivier, 1790)
(Coleoptera, Dryophthoridae) on the dwarf palm, Chamaerops humilis L. (Cocco et
al. 2019). Importantly, S. imbatus has been reported on > 90 host species and = 20
genera (de Jess Parra-Gil et al. 2020), which is one of the widest host ranges within
the Bruchinae. In view of its tropic spectrum, it has been classified as polyphagous, i.e.,
feeding in the seeds of various plant genera of different subfamilies (Ribeiro-Costa and

Establishment and new hosts of Stator limbatus in Europe 185

Almeida 2012; Yus-Ramos 2018). However, its host use is widely variable and it shows
local specialization depending on the diversity of available host species (Morse and Far-
rell 2005a, 2005b). ‘The establishment of S. /imbatus in Europe and new associations
with A. pycnantha and A. saligna required a redefinition and update of the bruchid host
range to facilitate further research on its potential adaptation and spread in Europe.
The exact definition of the host range of S. /imbatus is not trivial due to nomenclatural
issues within the family Fabaceae which have not been resolved (LPWG 2017). In ad-
dition, in a number of cases, the literature reported incorrect or partial names for the
host plants. The bibliographic search analysis allowed to extend the global host range
of S. limbatus to 111 species, in most part belonging to the mimosoid clade of the
subfamily Caesalpinioideae (Fabaceae) (LP WG 2017). Synonym issues were resolved,
e.g., Acacia diversifolia and Leucaena diversifolia both mentioned by Romero Gomez
et al (2009) and synonymized in Leucaena diversifolia (Schltdl.) Benth, and up-to-date
nomenclature provide the current and comprehensive overview of the feeding spec-
trum of S. dimbatus. However, some old or unconfirmed reports would require further
investigations, e.g., G. max, Wallaceodendron celebicum Koord., and Arachis hypogaea
L. (Brian 1932; Kingsolver 2004). Since no previous records were found in literature,
A. pycnantha and A. saligna are included in the present paper for the first time in the
host range of S. limbatus.

This report of establishment of S. /imbatus in Europe contributes to updating
the insect worldwide distribution, which now includes North and Central America
(native region), South America, South Africa, the Middle East, and southern Europe.
Future research is required on known and potential host species in order to investigate
its potential distribution and new host associations with native or non-native plant
species (Parry et al. 2013). Studies on suitable climatic conditions for S. limbatus
development will further assess the risks of spread in the Mediterranean Basin. Such
surveys should include also urban habitats, in which seed feeders are frequently found
(Branco et al. 2019).

Acknowledgements

The authors gratefully acknowledge Gianluigi Bacchetta (Biodiversity Conservation
Centre, University of Cagliari, Italy) for fruitful discussions and technical support, and
Roberto Mannu (University of Sassari) for statistical advice. This study was financially
supported, in part, by the Project ALIEM “Action pour Limiter les risques de diffu-
sion des espéces Introduites Envahissantes en Méditerranée” PC IFM 2014-2020 and
by RESTART-UNINUORO Project “Azioni per la valorizzazione delle risorse agro-
forestali della Sardegna centrale/Actions for the valorisation of agroforestry resources
in central Sardinia” Regione Autonoma della Sardegna, D.G.R. N. 29/1 del 7 June
2018—fondi FSC 2014-2020. AS, GB, and IF gratefully acknowledge University of
Sassari for the financial support through “Fondo di Ateneo per la Ricerca 2020”. The
authors have declared that no competing interests exist.

186 Arturo Cocco et al. / NeoBiota 70: 167—192 (2021)

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